LITAF, a BCL6 target gene, regulates autophagy in mature B-cell lymphomas

British Journal of Haematology

Volumn 162, Issue 5, 2013, Pages 621-630

  Bertolo, Cristina ^a   Roa, Sergio ^a   Sagardoy, Ainara ^a   Mena Varas, Maria ^a   Robles, Eloy F ^a   Martinez Ferrandis, Jose I ^a   Sagaert, Xavier ^b   Tousseyn, Thomas ^b   Orta, Alberto ^a   Lossos, Izidore S ^c   Amar, Salomon ^d   Natkunam, Yasodha ^e   Briones, Javier ^f   Melnick, Ari ^g   Malumbres, Raquel ^a   Martinez Climent, Jose A ^a  

^a UNIVERSITY OF NAVARRA   (Spain)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c UNIVERSITY OF MIAMI   (United States)

^d BOSTON UNIVERSITY   (United States)

^e STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^g WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Autophagy; B cells; Germinal centre; Non hodgkin lymphoma; Transcription factors

Indexed keywords

PROTEIN BCL 6;

ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; B CELL LYMPHOMA; BCL6 GENE; CONTROLLED STUDY; FOLLICULAR LYMPHOMA; GENE EXPRESSION; GENE REPRESSION; GERMINAL CENTER; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INTRON; LARGE CELL LYMPHOMA; LIPOPOLYSACCHARIDE INDUCED TUMOR NECROSIS FACTOR GENE; LYMPHOMA CELL; LYSOSOME; MARGINAL ZONE LYMPHOMA; NUCLEOTIDE SEQUENCE; OVERALL SURVIVAL; PRIORITY JOURNAL; SPLENIC MARGINAL ZONE LYMPHOMA;

AUTOPHAGY; B CELLS; GERMINAL CENTRE; NON-HODGKIN LYMPHOMA; TRANSCRIPTION FACTORS;

AUTOPHAGY; B-LYMPHOCYTE SUBSETS; CELL LINE, TUMOR; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTRONS; LYMPHOMA, B-CELL; NEOPLASM PROTEINS; NUCLEAR PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84881662796     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/bjh.12440     Document Type: Article

References (45)

1. Basso, K. & Dalla-Favera, R. (2010) BCL6: master regulator of the germinal center reaction and key oncogene in B cell lymphomagenesis. Advances in Immunology, 105, 193-210.
2. Beltran, E., Fresquet, V., Martinez-Useros, J., Richter-Larrea, J.A., Sagardoy, A., Sesma, I., Almada, L.L., Montes-Moreno, S., Siebert, R., Gesk, S., Calasanz, M.J., Malumbres, R., Rieger, M., Prosper, F., Lossos, I.S., Piris, M.A., Fernandez-Zapico, M.E. & Martinez-Climent, J.A. (2011) A cyclin-D1 interaction with BAX underlies its oncogenic role and potential as a therapeutic target in mantle cell lymphoma. Proceedings of the National Academy of Sciences of the United States of America, 108, 12461-12466.
3. Chen, W., Iida, S., Louie, D.C., Dalla-Favera, R. & Chaganti, R.S. (1998) Heterologous promoters fused to BCL6 by chromosomal translocations affecting band 3q27 cause its deregulated expression during B-cell differentiation. Blood, 91, 603-607.
4. Ci, W., Polo, J.M. & Melnick, A. (2008) B-cell lymphoma 6 and the molecular pathogenesis of diffuse large B-cell lymphoma. Current Opinion in Hematology, 15, 381-390.
5. Ci, W., Polo, J.M., Cerchietti, L., Shaknovich, R., Wang, L., Yang, S.N., Ye, K., Farinha, P., Horsman, D.E., Gascoyne, R.D., Elemento, O. & Melnick, A. (2009) The BCL6 transcriptional program features repression of multiple oncogenes in primary B cells and is deregulated in DLBCL. Blood, 113, 5536-5548.
6. Clark, M.R., Massenburg, D., Siemasko, K., Hou, P. & Zhang, M. (2004) B-cell antigen receptor signaling requirements for targeting antigen to the MHC class II presentation pathway. Current Opinion in Immunology, 16, 382-387.
7. Duy, C., Yu, J.J., Nahar, R., Swaminathan, S., Kweon, S.M., Polo, J.M., Valls, E., Klemm, L., Shojaee, S., Cerchietti, L., Schuh, W., Jäck, H.M., Hurtz, C., Ramezani-Rad, P., Herzog, S., Jumaa, H., Koeffler, H.P., de Alborán, I.M., Melnick, A.M., Ye, B.H. & Müschen, M. (2010) BCL6 is critical for the development of a diverse primary B cell repertoire. Journal of Experimental Medicine, 207, 1209-1221.
8. Eaton, H.E., Metcalf, J., Lacerda, A.F. & Brunetti, C.R. (2012) Accumulation of endogenous LITAF in aggresomes. PLoS ONE, 7, e30003.
9. Hubbard, V.M., Valdor, R., Patel, B., Singh, R., Cuervo, A.M. & Macian, F. (2010) Macroautophagy regulates energy metabolism during effector T cell activation. Journal of Immunology, 185, 7349-7357.
10. Klein, U. & Dalla-Favera, R. (2008) Germinal centres: role in B-cell physiology and malignancy. Nature Reviews Immunology, 8, 22-33.
11. Lee, S.M., Chin, L.S. & Li, L. (2012) Charcot-Marie-Tooth disease-linked protein SIMPLE functions with the ESCRT machinery in endosomal trafficking. Journal of Cell Biology, 199, 799-816.
12. Liang, X.H., Jackson, S., Seaman, M., Brown, K., Kempkes, B., Hibshoosh, H. & Levine, B. (1999) Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature, 402, 672-676.
13. Liu, J., Xing, H., Chen, Y., Wang, L., Wang, D., Rao, Q., Tang, K., Tian, Z., He, K., Wang, M. & Wang, J. (2012) PIG7, transactivated by AML1, promotes apoptosis and differentiation of leukemia cells with AML1-ETO fusion gene. Leukemia, 26, 117-126.
14. MacLennan, I.C., Gulbranson-Judge, A., Toellner, K.M., Casamayor-Palleja, M., Chan, E., Sze, D.M., Luther, S.A. & Orbea, H.A. (1997) The changing preference of T and B cells for partners as T-dependent antibody responses develop. Immunological Reviews, 156, 53-66.
15. Malumbres, R., Chen, J., Tibshirani, R., Johnson, N.A., Sehn, L.H., Natkunam, Y., Briones, J., Advani, R., Connors, J.M., Byrne, G.E., Levy, R., Gascoyne, R.D. & Lossos, I.S. (2008) Paraffin-based 6-gene model predicts outcome in diffuse large B-cell lymphoma patients treated with R-CHOP. Blood, 111, 5509-5514.
16. Malumbres, R., Sarosiek, K.A., Cubedo, E., Ruiz, J.W., Jiang, X., Gascoyne, R.D., Tibshirani, R. & Lossos, I.S. (2009) Differentiation stage-specific expression of microRNAs in B lymphocytes and diffuse large B-cell lymphomas. Blood, 113, 3754-3764.
17. Mestre-Escorihuela, C., Rubio-Moscardo, F., Richter, J.A., Siebert, R., Climent, J., Fresquet, V., Beltran, E., Agirre, X., Marugan, I., Marin, M., Rosenwald, A., Sugimoto, K.J., Wheat, L.M., Karran, E.L., Garcia, J.F., Sanchez, L., Prosper, F., Staudt, L.M., Pinkel, D., Dyer, M.J. & Martinez-Climent, J.A. (2007) Homozygous deletions localize novel tumor suppressor genes in B-cell lymphomas. Blood, 109, 271-280.
18. Mizushima, N., Yoshimori, T. & Levine, B. (2010) Methods in mammalian autophagy research. Cell, 140, 313-326.
19. Moriwaki, Y., Begum, N.A., Kobayashi, M., Matsumoto, M., Toyoshima, K. & Seya, T. (2001) Mycobacterium bovis Bacillus Calmette-Guerin and its cell wall complex induce a novel lysosomal membrane protein, SIMPLE, that bridges the missing link between lipopolysaccharide and p53-inducible gene, LITAF(PIG7), and estrogen-inducible gene, EET-1. Journal of Biological Chemistry, 276, 23065-23076.
20. Munz, C. (2009) Enhancing immunity through autophagy. Annual Review of Immunology, 27, 423-449.
21. Myokai, F., Takashiba, S., Lebo, R. & Amar, S. (1999) A novel lipopolysaccharide-induced transcription factor regulating tumor necrosis factor alpha gene expression: molecular cloning, sequencing, characterization, and chromosomal assignment. Proceedings of the National Academy of Sciences of the United States of America, 96, 4518-4523.
22. Parekh, S., Polo, J.M., Shaknovich, R., Juszczynski, P., Lev, P., Ranuncolo, S.M., Yin, Y., Klein, U., Cattoretti, G., Dalla Favera, R., Shipp, M.A. & Melnick, A. (2007) BCL6 programs lymphoma cells for survival and differentiation through distinct biochemical mechanisms. Blood, 110, 2067-2074.
23. Phan, R.T. & Dalla-Favera, R. (2004) The BCL6 proto-oncogene suppresses p53 expression in germinal-centre B cells. Nature, 432, 635-639.
24. Phan, R.T., Saito, M., Basso, K., Niu, H. & Dalla-Favera, R. (2005) BCL6 interacts with the transcription factor Miz-1 to suppress the cyclin-dependent kinase inhibitor p21 and cell cycle arrest in germinal center B cells. Nature Immunology, 6, 1054-1060.
25. Polo, J.M., Dell'Oso, T., Ranuncolo, S.M., Cerchietti, L., Beck, D., Da Silva, G.F., Prive, G.G., Licht, J.D. & Melnick, A. (2004) Specific peptide interference reveals BCL6 transcriptional and oncogenic mechanisms in B-cell lymphoma cells. Nature Medicine, 10, 1329-1335.
26. Polyak, K., Xia, Y., Zweier, J.L., Kinzler, K.W. & Vogelstein, B. (1997) A model for p53-induced apoptosis. Nature, 389, 300-305.
27. Qu, X., Yu, J., Bhagat, G., Furuya, N., Hibshoosh, H., Troxel, A., Rosen, J., Eskelinen, E.L., Mizushima, N., Ohsumi, Y., Cattoretti, G. & Levine, B. (2003) Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. Journal of Clinical Investigation, 112, 1809-1820.
28. Ranuncolo, S.M., Polo, J.M., Dierov, J., Singer, M., Kuo, T., Greally, J., Green, R., Carroll, M. & Melnick, A. (2007) Bcl-6 mediates the germinal center B cell phenotype and lymphomagenesis through transcriptional repression of the DNA-damage sensor ATR. Nature Immunology, 8, 705-714.
29. Ranuncolo, S.M., Wang, L., Polo, J.M., Dell'Oso, T., Dierov, J., Gaymes, T.J., Rassool, F., Carroll, M. & Melnick, A. (2008) BCL6-mediated attenuation of DNA damage sensing triggers growth arrest and senescence through a p53-dependent pathway in a cell context-dependent manner. Journal of Biological Chemistry, 283, 22565-22572.
30. Richter-Larrea, J.A., Robles, E.F., Fresquet, V., Beltran, E., Rullan, A.J., Agirre, X., Calasanz, M.J., Panizo, C., Richter, J.A., Hernandez, J.M., Roman-Gomez, J., Prosper, F. & Martinez-Climent, J.A. (2010) Reversion of epigenetically mediated BIM silencing overcomes chemoresistance in Burkitt lymphoma. Blood, 116, 2531-2542.
31. Rosenwald, A., Wright, G., Chan, W.C., Connors, J.M., Campo, E., Fisher, R.I., Gascoyne, R.D., Muller-Hermelink, H.K., Smeland, E.B., Giltnane, J.M., Hurt, E.M., Zhao, H., Averett, L., Yang, L., Wilson, W.H., Jaffe, E.S., Simon, R., Klausner, R.D., Powell, J., Duffey, P.L., Longo, D.L., Greiner, T.C., Weisenburger, D.D., Sanger, W.G., Dave, B.J., Lynch, J.C., Vose, J., Armitage, J.O., Montserrat, E., López-Guillermo, A., Grogan, T.M., Miller, T.P., LeBlanc, M., Ott, G., Kvaloy, S., Delabie, J., Holte, H., Krajci, P., Stokke, T., Staudt, L.M. & Project, L.L.M.P. (2002) The use of molecular profiling to predict survival after chemotherapy for diffuse large-B-cell lymphoma. New England Journal of Medicine, 346, 1937-1947.
32. Saito, M., Novak, U., Piovan, E., Basso, K., Sumazin, P., Schneider, C., Crespo, M., Shen, Q., Bhagat, G., Califano, A., Chadburn, A., Pasqualucci, L. & Dalla-Favera, R. (2009) BCL6 suppression of BCL2 via Miz1 and its disruption in diffuse large B cell lymphoma. Proceedings of the National Academy of Sciences of the United States of America, 106, 11294-11299.
33. Shaffer, A.L., Lin, K.I., Kuo, T.C., Yu, X., Hurt, E.M., Rosenwald, A., Giltnane, J.M., Yang, L., Zhao, H., Calame, K. & Staudt, L.M. (2002) Blimp-1 orchestrates plasma cell differentiation by extinguishing the mature B cell gene expression program. Immunity, 17, 51-62.
34. Somandin, C., Gerber, D., Pereira, J.A., Horn, M. & Suter, U. (2012) LITAF (SIMPLE) regulates Wallerian degeneration after injury but is not essential for peripheral nerve development and maintenance: implications for Charcot-Marie-Tooth disease. Glia, 60, 1518-1528.
35. Strawbridge, A.B. & Blum, J.S. (2007) Autophagy in MHC class II antigen processing. Current Opinion in Immunology, 19, 87-92.
36. Street, V.A., Bennett, C.L., Goldy, J.D., Shirk, A.J., Kleopa, K.A., Tempel, B.L., Lipe, H.P., Scherer, S.S., Bird, T.D. & Chance, P.F. (2003) Mutation of a putative protein degradation gene LITAF/SIMPLE in Charcot-Marie-Tooth disease 1C. Neurology, 60, 22-26.
37. Takeuchi, H., Kondo, Y., Fujiwara, K., Kanzawa, T., Aoki, H., Mills, G.B. & Kondo, S. (2005) Synergistic augmentation of rapamycin-induced autophagy in malignant glioma cells by phosphatidylinositol 3-kinase/protein kinase B inhibitors. Cancer Research, 65, 3336-3346.
38. Tang, X., Marciano, D.L., Leeman, S.E. & Amar, S. (2005) LPS induces the interaction of a transcription factor, LPS-induced TNF-alpha factor, and STAT6(B) with effects on multiple cytokines. Proceedings of the National Academy of Sciences of the United States of America, 102, 5132-5137.
39. Tang, X., Metzger, D., Leeman, S. & Amar, S. (2006) LPS-induced TNF-alpha factor (LITAF)-deficient mice express reduced LPS-induced cytokine: Evidence for LITAF-dependent LPS signaling pathways. Proceedings of the National Academy of Sciences of the United States of America, 103, 13777-13782.
40. Tunyaplin, C., Shaffer, A.L., Angelin-Duclos, C.D., Yu, X., Staudt, L.M. & Calame, K.L. (2004) Direct repression of prdm1 by Bcl-6 inhibits plasmacytic differentiation. Journal of Immunology, 173, 1158-1165.
41. Vicente-Dueñas, C., Fontán, L., Gonzalez-Herrero, I., Romero-Camarero, I., Segura, V., Aznar, M.A., Alonso-Escudero, E., Campos-Sanchez, E., Ruiz-Roca, L., Barajas-Diego, M., Sagardoy, A., Martinez-Ferrandis, J.I., Abollo-Jimenez, F., Bertolo, C., Peñuelas, I., Garcia-Criado, F.J., García-Cenador, M.B., Tousseyn, T., Agirre, X., Prosper, F., Garcia-Bragado, F., McPhail, E.D., Lossos, I.S., Du, M.Q., Flores, T., Hernandez-Rivas, J.M., Gonzalez, M., Salar, A., Bellosillo, B., Conde, E., Siebert, R., Sagaert, X., Cobaleda, C., Sanchez-Garcia, I. & Martinez-Climent, J.A. (2012) Expression of MALT1 oncogene in hematopoietic stem/progenitor cells recapitulates the pathogenesis of human lymphoma in mice. Proceedings of the National Academy of Sciences of the United States of America, 109, 10534-10539.
42. Watanabe, K., Ichinose, S., Hayashizaki, K. & Tsubata, T. (2008) Induction of autophagy by B cell antigen receptor stimulation and its inhibition by costimulation. Biochemical and Biophysical Research Communications, 374, 274-281.
43. Watsuji, T., Okamoto, Y., Emi, N., Katsuoka, Y. & Hagiwara, M. (1997) Controlled gene expression with a reverse tetracycline-regulated retroviral vector (RTRV) system. Biochemical and Biophysical Research Communications, 234, 769-773.
44. Yue, Z., Jin, S., Yang, C., Levine, A.J. & Heintz, N. (2003) Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proceedings of the National Academy of Sciences of the United States of America, 100, 15077-15082.
45. Zhou, J., Yang, Z., Tsuji, T., Gong, J., Xie, J., Chen, C., Li, W., Amar, S. & Luo, Z. (2011) LITAF and TNFSF15, two downstream targets of AMPK, exert inhibitory effects on tumor growth. Oncogene, 30, 1892-1900.